THE FORMATION OF HABITS The implicit supervision of the basal ganglia
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1 THE FORMATION OF HABITS The implicit supervision of the basal ganglia MEROPI TOPALIDOU 12e Colloque de Société des Neurosciences Montpellier May 1922, 2015
2 THE FORMATION OF HABITS The implicit supervision of the basal ganglia MEROPI TOPALIDOU 12e Colloque de Société des Neurosciences Montpellier May 1922, 2015
3 THE FORMATION OF HABITS The implicit supervision of the basal ganglia MEROPI TOPALIDOU 12e Colloque de Société des Neurosciences Montpellier May 1922, 2015
4 GoalDirected Actions VS Habits Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
5 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
6 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
7 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome sensitive to devaluation of the outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
8 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome direct initiation of responding by stimulus and/or context presentation sensitive to devaluation of the outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
9 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome direct initiation of responding by stimulus and/or context presentation sensitive to devaluation of the outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
10 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome sensitive to devaluation of the outcome direct initiation of responding by stimulus and/or context presentation resistant to devaluation of the outcome Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
11 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome sensitive to devaluation of the outcome direct initiation of responding by stimulus and/or context presentation resistant to devaluation of the outcome behavior adjusts to reflect the new value of the outcome that the action would obtain Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
12 GoalDirected Actions VS Habits initiation of response is under direct control of the current value of outcome sensitive to devaluation of the outcome direct initiation of responding by stimulus and/or context presentation resistant to devaluation of the outcome behavior adjusts to reflect the new value of the outcome that the action would obtain habits persist even if the reward becomes less attractive or if the action is not necessary to earn the reward. Belin et al. (2008), Yin (2008), Foerde & Shohamy (2011), Doll et al. (2012)
13 Cortex Basal Ganglia Novel behaviors require attention and flexible thinking and therefore are dependent on cortex, whereas automatic behaviors has been assumed to be primarily mediated by subcortical structures. Much evidence suggests however, that subcortical structures, such as the striatum, make significant contributions to initial learning. More recently, evidence has been accumulating that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensori striatum are more active after automaticity has developed. At the same time, other recent reports suggest that automatic behaviors are striatum and dopamineindependent, and may be mediated entirely within cortex. Resolving this apparent conflict should be a major goal of future research. These ideas led to the theory that dominated the 20th century: Novel behaviors require attention and flexible thinking and therefore are dependent on cortex, whereas automatic behaviors require neither of these and so are not mediated primarily by cortex. Instead, it has long been assumed that automatic behaviors are primarily mediated by subcortical structures.
14 Cortex Basal Ganglia Goal Directed actions go here Cortex leads decision once learned Habits go there BG teach cortex during learning phase Daw, Niv & Dayan (2005) Ashby, Turner & Horvitz (2010) Novel behaviors require attention and flexible thinking and therefore are dependent on cortex, whereas automatic behaviors has been assumed to be primarily mediated by subcortical structures. Much evidence suggests however, that subcortical structures, such as the striatum, make significant contributions to initial learning. More recently, evidence has been accumulating that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensori striatum are more active after automaticity has developed. At the same time, other recent reports suggest that automatic behaviors are striatum and dopamineindependent, and may be mediated entirely within cortex. Resolving this apparent conflict should be a major goal of future research. These ideas led to the theory that dominated the 20th century: Novel behaviors require attention and flexible thinking and therefore are dependent on cortex, whereas automatic behaviors require neither of these and so are not mediated primarily by cortex. Instead, it has long been assumed that automatic behaviors are primarily mediated by subcortical structures.
15 Outline Experiment Computational model Results
16 Experimental setup Two monkeys, simple twoarmed bandit task with P=0.75 and P=0.25. Habitual condition (known stimuli pair, same every day) Novel condition (unfamiliar stimuli pair, new every day) Habitual Condition Trial start Cue presentation Go signal Decision Reward Trial stop Prelearned cues Novel Condition Novel cues (every day) s 1.5s 1.0s 1.5s 1.0s 1.5s Time Piron et al. (submitted)
17 Experimental results 1.0 Mean success rate saline HC Number of trials NC Mean success rate * HC NC Saline Mean of first 25 trials * HC NC Saline Mean of last 25 trials Piron et al. (submitted)
18 Experimental results Muscimol injection in GPi disrupts learning in novel conditions (NC) but performances remains intact (but slower) in habitual conditions (HC). Mean success rate saline muscimol HC Number of trials NC Mean success rate * * * * HC NC HC NC Saline Muscimol Mean of last 25 trials Piron et al. (submitted)
19 Experimental conclusion If habits were stored in basal ganglia, monkeys would not achieve peak performances in muscimol conditions for familiar stimuli. If habits were learned in cortex, monkeys would be able to reach peak performances in muscimol conditions for unfamiliar stimuli. 1.0 Mean success rate saline muscimol HC Number of trials NC Piron et al. (submitted)
20 Computational model Neural Network Neuron Rate model Two segregated loops: Cognitive loop allows to choose a shape Motor loop allows to reach a shape External current 2 External current Cortex + External current Cortex associative (4x4 units) Cortex GPe HYPERDIRECT PATHWAY Striatum DIRECT PATHWAY Striatum associative (4x4 units) 3 Striatum GPe INDIRECT PATHWAY STN GPi GPi STN Thalamus Thalamus Topalidou et al. (in prep.)
21 Corticobasal competition Cognitive decision has to intervene in decision. Cortical decision Thanks to lateral competition, cortex can take a decision without interaction with BG. External current External current External current Cortex 2 + Cortex associative (4x4 units) Cortex CorticoBasal decision GPe HYPERDIRECT PATHWAY Striatum DIRECT PATHWAY Striatum associative (4x4 units) 3 Striatum GPe INDIRECT PATHWAY STN GPi GPi STN Thalamus Thalamus Topalidou et al. (in prep.)
22 Acting is learning Learning occurs at three different places simultaneously. 1 & 2 Hebbian learning 3 Reinforcement learning Cortex learns to reproduce previous repertories, regardless of whether or not are appropriate (HL). Fast basal ganglia trialanderror learning (RL) biases slow cortical one (HL) ensuring that the correct behavior is produced. Hélie et al. (2014) External current 2 External current GPe INDIRECT PATHWAY Cortex HYPERDIRECT PATHWAY STN Striatum DIRECT PATHWAY + GPi Thalamus External current Cortex associative (4x4 units) Striatum associative (4x4 units) GPi Thalamus Striatum Cortex 3 STN GPe Topalidou et al. (in prep.)
23 Computational results Intact model peak performances on familiar conditions can learn novel conditions Lesioned model (GPi) peak performances on familiar conditions cannot learn novel conditions External current + External current External current (Monkey results) GPe INDIRECT PATHWAY Cortex HYPERDIRECT PATHWAY STN 2 Striatum DIRECT PATHWAY GPi Thalamus Cortex associative (4x4 units) Striatum associative (4x4 units) GPi Thalamus Striatum Cortex 3 STN GPe Mean success rate saline muscimol HC Number of trials NC Topalidou et al. (in prep.)
24 Sensitivity to reward devaluation
25 Conclusion The acquisition and the expression of habits are two entangled processes that can be dissociated experimentally. This experimental dissociation sheds light on the nature of the interaction between the basal ganglia and the cortex and their respective role in the initial formation and the later expression of habits. The model suggests that the basal ganglia implicitly supervises the cortex where habits are actually stored, but the cortex cannot learn them on its own. In the future, the model will be tested in different protocols in order to ensure the accuracy of its predictions.
26 Acknowledgements Nicolas Rougier T. Boraud C. Piron D. Kase A. Leblois
27 Acknowledgements Nicolas Rougier T. Boraud C. Piron D. Kase A. Leblois
28 Acknowledgements Nicolas Rougier T. Boraud C. Piron D. Kase A. Leblois
29 Acknowledgements Nicolas Rougier T. Boraud C. Piron D. Kase A. Leblois
30 Acknowledgements Nicolas Rougier T. Boraud C. Piron D. Kase A. Leblois
31
32 Reaction period (ms) * * * * HC NC HC NC Saline Muscimol
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